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2023 Article 3015
2023 Article 3015
2023 Article 3015
Abstract
Background Tooth loss may be a surrogate for systemic health and aging. However, no previous studies have
systematically assessed multiple outcomes relevant to aging trajectory in this area, and many important confounders
were not adjusted in most previous studies. This study aims to prospectively evaluate the associations of complete
tooth loss (edentulism) with broad markers of sarcopenia, cognitive impairment and mortality.
Methods Data were derived from the China Health and Retirement Longitudinal Study, a nationally representative
household study of the Chinese population aged 45 years and older. Multivariate Weibull proportional hazards
regression was used to assess the association between edentulism with sarcopenia and all-cause mortality. Average
changes in cognitive function by edentulism was estimated by mixed-effects linear regression models.
Results During the 5-year follow-up, the prevalence of edentulism among adults aged 45 and over was 15.4%.
Participants with edentulism had a greater decline in cognitive function compared to those without (β=-0.70, 95%CI:-
1.09, -0.31, P < 0.001). The association of edentulism and all-cause mortality for 45–64 age group (HR = 7.50, 95%CI:
1.99, 28.23, P = 0.003), but not statistically significant for the ≥ 65 age group (HR = 2.37, 95%CI: 0.97, 5.80, P = 0.057).
Effects of edentulism on sarcopenia are statistically significant for all age groups (45–64 age group: HR = 2.15, 95%CI:
1.27, 3.66, P = 0.005; ≥65 age group: HR = 2.15, 95%CI: 1.27, 3.66, P = 0.002).
Conclusions These findings could have important clinical and public health implications, as tooth loss is a quick and
reproducible measurement that could be used in clinical practice for identifying persons at risk of accelerated aging
and shortened longevity, and who may benefit most from intervention if causality is established.
Keywords Cognitive impairment, Edentulism, Longitudinal analysis, Mortality, Sarcopenia
†
Yang Li and Chuan-Long Huang authors contribute equally.
*Correspondence:
Ying Sun
yingsun@ahmu.edu.cn
Xin Chen
chenxinkq2672@126.com
1
Key Laboratory of Oral Diseases Research of Anhui Province,
Stomatologic Hospital & College, Anhui Medical University, Hefei, China
2
Department of Maternal, Child & Adolescent Health, School of Public
Health, Anhui Medical University, 81th Meishan Road, Hefei,
Anhui Province 230032, China
© The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use,
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Li et al. BMC Oral Health (2023) 23:333 Page 2 of 10
cognitive function score varied from 0 to 30, with higher to the suggestion of AWGS 2019, the cut-off points for
values meaning better cognitive function [18]. low handgrip strength are < 18 kg in women and < 28 kg
in men.
Assessment of sarcopenia
According to the AWGS criteria, sarcopenia was diag- Measurement of muscle mass The muscle mass was esti-
nosed if participants had low muscle mass plus low mus- mated by the appendicular skeletal muscle mass (ASM)
cle strength or low physical performance [19]. using a previously validated anthropometric equation in a
Chinese population [20]:
Measurement of muscle strength AWGS 2019 recom-
mends using handgrip strength to indicate skeletal mus- 0.193*weight + 0.107*height - 4.156*sex1 -
(1)
cle strength. Handgrip strength (kg) was measured in the 0.037*death_age - 2.631
dominant hand and non-dominant hand, with the par-
ticipant squeezing a YuejianTM WL-1000 dynamometer The height, body weight and age were measured in cen-
(Nantong Yuejian Physical Measure-ment Instrument timeters, kilograms and years, respectively. For sex, the
Co., Ltd., Nantong, China) as hard as possible. According value 1 represented men, and the value 2 represented
Li et al. BMC Oral Health (2023) 23:333 Page 4 of 10
women. The agreement of the ASM equation model factors including smoking, drinking, activities of daily
and dual X-ray absorptiometry (DXA) was strong. After living, sleep duration and body mass index; and Model 3
calculating the ASM, the height-adjusted muscle mass was additionally adjusted for self-reported medical his-
(ASM/Ht2) was calculated using the ASM divided by tory (hypertension, diabetes, respiratory illnesses, stroke
the square of the height in meters. The ASM/Ht2 val- and heart disease and other chronic illnesses at Wave 4).
ues of < 5.63 kg/m2 in women and < 7.05 kg/m2 in men Sensitivity analysis was conducted in subgroups of pop-
were considered as low muscle mass. In terms of physi- ulation without stroke or heart diseases to examine the
cal performance, the gait speed and the chair stand test stability of results.
were performed using the method described by Wu et al. Multivariate Weibull proportional hazards regression
[21]0.10 Further details about the definitions for sarco- model before and after adjusting for confounding factors
penia components in the CHARLS have been described (sociodemographic factors, health-related factors, and
previously.10 According to AWGS 2019, the criteria for self-reported medical history) were used to estimate the
low physical performance are 6-m walk < 1.0 m/s, or associations between edentulism with all-cause mortality
5-time chair stand test ≥ 12 s [19]. and sarcopenia. Hazard ratios (HRs) and 95% CIs were
reported for both unadjusted and covariate-adjusted
All-cause mortality models. Statistical significance was set at two-sided
The death information in CHARLS was determined by P < 0.05. Analyses were performed using STATA v15 sta-
the exit interview status (alive or dead) of participants in tistical software.
Waves 3 and Wave 4. Considering the exact time of death
was not recorded, the median of the two follow-up times Results
was used as the survival time. The characteristics of study participants according to
edentulous groups are presented in Table 1. The mean
Covariates age of the 16 501 participants was 58.8 (standard devia-
We selected covariates that may confound the relation- tion [SD], 9.5) years, and 51.2% were women. Nearly 2/3
ship based on a review of literature. The selected covari- (66.4%) of participants received primary education or
ates should have an impact on the physical fragility, less.
cognitive impairment, and overall mortality and been The prevalence of edentulism among adults aged 45
collected in the CHARLS. Because the sample size of this and over was 15.4% (2537/16,501), with 10.1% for age
study is large and statistical power is strong, we included group 45–64 years, 25.6% for age group 65–74 years
as many covariates as possible to minimize the poten- and 44.2% for age group 75 and over. Compared to those
tial confounding effect. The covariates for our analyses without edentulism, edentulous participants were older,
included sociodemographic characteristics (age, sex, being female, less educated, and had lower BMI, lower
household income, education, occupation status, marital household income, and lower alcohol use (all Ps < 0.001).
status and residence), routine physical checkup (weigh, As shown in Table 1, compared to those without eden-
height, and blood pressure), lifestyle behaviors (smok- tulism, the prevalence of high blood pressure at 2013
ing, alcohol drinking and sleep duration), self-reported wave was significantly higher among participants with
chronic conditions (hypertension, diabetes/hyperglycae- edentulism (P < 0.001). The prevalence of heart diseases
mia, cancer, lung disease, stroke, heart disease, psycho- was similar at 2013 between the two groups (14.1% vs.
logical disease, arthritis, liver disease, kidney disease, 13.2%, P = 0.257), but significantly increased at 2015
digestive disease, asthma and memory-related disease). (20.2% vs. 17.6%, P = 0.004) and 2018 (25.1% vs. 21.1%,
Details on the precision of the covariates are provided in P < 0.001) among elder population with edentulism.
the appendix. Cognitive function score declined with age during the
follow-up period in all participants (Table 2). Partici-
Statistical analyses pants with edentulism had a greater decline compared
Baseline characteristics of participant with and without to those without. The associations remained significant
edentulism were compared using χ2 tests for categorical after adjusted prevalent cardiovascular diseases, e.g.
measures and t tests for continuous measures. Statistical high blood pressure, diabetes, stroke and heart disease
analysis was performed from April to August, 2022. Aver- at Wave 4 (β=-0.70, 95%CI:-1.09, -0.31, P < 0.001). Results
age changes in cognitive function over Wave 2 to Wave 4 from sensitivity analyses excluding participants with
by edentulism status was estimated using mixed-effects baseline cardiovascular diseases were qualitatively simi-
linear regression models. We ran three incremental mod- lar (β=-0.68, 95%CI: -1.10, -0.26, P = 0.001).
els: Model 1 was adjusted for sociodemographic fac- Table 3 shows the associations between edentulism
tors (age, sex, household annual income and education); with mortality and sarcopenia from the random-inter-
Model 2 was additionally adjusted for health-related cept Weibull hazard models, respectively. The mortality
Li et al. BMC Oral Health (2023) 23:333 Page 5 of 10
Table 1 Characteristics of study participants by edentulism at 2013 in China Health and Retirement Longitudinal Study
Characteristics Total sample Edentulism during 2013–2018 P-values
(n = 16,501)
Yes (n = 2537) No (n = 13,964)
Age at 2013 (years), mean (SD) 16,501 65.5 ± 9.9 57.6 ± 8.8 < 0.001
45–64 years 12,271 1244 (10.1) 11,027 (89.9) < 0.001
65–74 years 3104 795 (25.6) 2309 (74.4)
>=75 years 1126 498 (44.2) 628 (55.8)
Female, n (%) 0.001
Female 8449 1374 (16.3) 7075 (83.7)
Male 8052 1163 (14.4) 6889 (85.6)
Education at 2013, n (%) 14,403 < 0.001
Primary or less 9570 1781 (18.6) 7789 (81.4)
Lower secondary 3123 314 (10.1) 2809 (89.9)
Upper secondary & vocational 1500 99 (6.6) 1401 (93.4)
Tertiary 210 16 (7.6) 194 (92.4)
Household income at 2013, mean (SD) 9377 10376.7 ± 12498.0 18941.3 ± 24766.4 < 0.001
BMI at 2013, mean (SD) 10,145 23.1 ± 5.2 24.1 ± 3.7 < 0.001
Current smoke at 2013, n (%) 13,943 520 (25.4) 3215 (27.0) 0.145
Alcohol use at 2013, n (%) 13,943 565 (27.6) 4055 (34.1) < 0.001
High blood pressure at 2013, n (%) 13,277 580 (26.4) 2434 (22.0) < 0.001
Dentures, n(%) 14,303 516 (61.8) 4020 (29.8) < 0.001
Stroke, n (%)
W2 (2013) 13,253 72 (3.3) 304 (2.8) 0.181
W3 (2015) 13,810 95 (4.5) 450 (3.8) 0.150
W4 (2018) 13,963 192 (9.4) 932 (7.8) 0.019
Heart diseases, n (%)
W2 (2013) 13,218 310 (14.1) 1451 (13.2) 0.257
W3 (2015) 13,719 425 (20.2) 2044 (17.6) 0.004
W4 (2018) 13,961 514 (25.1) 2516 (21.1) < 0.001
Global cognition score, mean (SD)
W2 (2013) 10,286 13.9 ± 4.9 15.5 ± 4.6 < 0.001
W3 (2015) 11,294 13.1 ± 4.8 14.9 ± 4.7 < 0.001
W4 (2018) 8575 13.8 ± 5.2 15.7 ± 5.0 < 0.001
Sarcopenia at 2015, n (%) 7666 131 (11.3) 242 (3.7) < 0.001
Death at 2018, n (%) 16,256 217 (9.5) 496 (3.6) < 0.001
incidence rate among older adults with edentulism was 1.70-times higher among edentulous participants, com-
19.9 per 1000 person-years (95%CI: 17.4, 22.7), compared pared with control groups (mortality: 95%CI: 1.39,
to 8.1 per 1000 person-years (95%CI: 7.4, 8.8) among 5.98, P = 0.004; sarcopenia: 95%CI: 1.32, 2.20, P < 0.001)
control group. Similarly, the incidence of sarcopenia dur- (Table 3; Fig. 2).
ing 2013 to 2015 waves was significantly higher in eden- We age-stratify our analysis by separately examining
tulous participants (28.3 cases per 1000 person years, each of the two age groups, 45–64 years and 65 years or
95%CI: 22.8, 35.1) compared to their counterparts from older. The results confirm the association of edentulism
control group (10.4 cases per 1000 person years, 95%CI: and all-cause mortality for 45–64 age group (HR = 7.50,
9.3, 11.7). 95%CI: 1.99, 28.23, P = 0.003), but not statistically signifi-
We calculated two regression models—the null model cant for the ≥ 65 age group (HR = 2.37, 95%CI: 0.97, 5.80,
is an empty model without any covariates, and the full P = 0.057). Effects of edentulism on sarcopenia are sta-
model includes all covariate—gender, educational level, tistically significant for all age groups (45–64 age group:
BMI, baseline cardiovascular diseases, diabetes, respi- HR = 2.15, 95%CI: 1.27, 3.66, P = 0.005; ≥65 age group:
ratory illnesses and other chronic morbidities, physi- HR = 2.15, 95%CI: 1.27, 3.66, P = 0.002).
cal activity, current smoking and drinking behavior, and
household income. In both models, the variation in mor-
tality and sarcopenia risk was statistically significant. The
median hazard of mortality and sarcopenia is 2.88- and
Li et al. BMC Oral Health (2023) 23:333 Page 6 of 10
Table 2 Average changes in cognitive function during 2013 to 2018 waves by edentulism in CHARLS using mixed-effects linear
regression models
Variables β-coefficient (95% confidence) Interval),
cognitive function during Wave 2 to Wave
4
Model 1 a Model 2 a Model 3 a
Total sample
Edentulism
No Reference Reference Reference
Yes -0.50 (-68, -0.33) ¶ -0.75 (-1.13, -0.70 (-1.09,
-0.38) ¶ -0.31) ¶
Age -0.11 (-0.12, -0.12 (-0.14, -0.12 (-0.14,
-0.10) ¶ -0.11) ¶ -0.11) ¶
Female -0.53 (-0.65, 0.42) ¶ -1.02 (-1.31, -1.00 (-1.31,
-0.74) ¶ -0.70) ¶
Education
Primary or less Reference Reference Reference
Lower secondary 2.92 (2.78, 3.06) ¶ 3.04 (2.74, 3.15 (2.84,
3.35) ¶ 3.47) ¶
Upper secondary 4.41 (4.23, 4.59) ¶ 4.50 (4.05, 4.64 (4.17,
4.94) ¶ 5.11) ¶
Tertiary 5.79 (5.38, 6.21) ¶ 6.27 (4.99, 6.31 (4.89,
7.54) ¶ 7.73) ¶
Participants without stroke or heart diseases at Wave 2
Edentulism
No Reference Reference Reference
Yes -0.56 (-0.89, -0.70 (-1.12, -0.68 (-1.10,
-0.23) § -0.28) § -0.26) §
a
Model 1 was adjusted for age, sex, household annual income and education; Model 2 was further adjusted for smoking, alcohol drinking, sleep duration, body mass
index and dentures; in Model 3, hypertension, diabetes, respiratory illnesses, stroke and heart disease and other chronic illnesses at Wave 4 were added
Table 3 Association of edentulism with mortality and sarcopenia estimated by random-intercept Weibull hazard models
Cases Incidence Rate (95%CI), per Hazard Ratio / Odds Ratio a
1000 Person-Years Model 1 Model 2
Incidence of death at Wave 4
Total
No edentulism group 496 8.1 (7.4, 8.8) Reference Reference
Edentulism group 217 19.9 (17.4, 22.7) 2.52 (2.15, 2.95) ¶ 2.88 (1.39, 5.98) §
Female 502 11.8 (10.8, 12.9) 0.32 (0.12, 0.81) *
Education
Primary or less 687 12.8 (11.9, 13.8) - Reference
Lower secondary 127 7.4 (6.2, 8.8) - 0.51 (0.15, 1,74)
Upper secondary and higher 52 5.5 (4.2, 7.2) - 0.80 (0.17, 3.69)
Aged 45–64
No edentulism group 199 4.2 (3.6, 4.8) Reference Reference
Edentulism group 34 6.2 (4.4, 8.6) 2.52 (2.15, 2.95) ¶ 7.50 (1.99, 28.23) §
Aged 65 or older
No edentulism group 297 19.4 (3.6, 24.4) Reference Reference
Edentulism group 183 33.8 (29.3, 39.1) 1.59 (1.32, 1.91) ¶ 2.37 (0.97, 5.80)
Incidence of sarcopenia at Wave 3
Total
No edentulism group 291 10.4 (9.3, 11.7) Reference Reference
Edentulism group 82 28.3 (22.8, 35.1) 3.37 (2.72, 4.17) ¶ 1.70 (1.32, 2.20) ¶
Female 287 16.7 (14.8, 18.7) 1.04 (0.77, 1.42)
Education
Primary or less 442 21.2 (19.3, 23.2) - Reference
Lower secondary 37 5.6 (4.0, 7.7) - 0.43 (0.25, 0.75) §
Upper secondary and higher 14 3.9 (2.3, 6.6) - 0.46 (0.21, 1.04)
Aged 45–64
No edentulism group 74 3.9 (3.1, 4.9) Reference Reference
Edentulism group 23 10.6 (7.1, 16.0) 3.22 (2.01, 5.16) ¶ 2.15 (1.27, 3.66) §
Aged 65 or older
No edentulism group 168 30.3 (26.1, 35.2) Reference Reference
Edentulism group 108 49.8 (41.2, 60.1) 1.65 (1.30, 2.11) ¶ 1.58 (1.19, 2.09) §
a
Model 1 was unadjusted for covariates; Model 2 was adjusted for age, sex, education, household annual income, smoking, alcohol drinking, sleep duration,
dentures, body mass index, hypertension, diabetes, respiratory illnesses, stroke and heart disease and other chronic illnesses at Wave 4
Several previous studies have evaluated whether health interventions might lead to reductions in early
edentulism and partial edentulism may be predictive of death.
shortened longevity [30–34], mostly conducted in high- Our findings demonstrated a consistent association
and upper-middle-income countries, which revealed between edentulism and sarcopenia in both community-
small association. Our study has further extended such dwelling middle-aged and older populations, suggesting
associations, indicating that late middle-aged adults that the association between edentulism with declining
(45–64 yeas) with edentulism presented a substantially muscle strength and muscle mass over time is robust.
(7.5-times) higher risk for all-cause mortality than the However, there is emerging evidence that tooth loss is
reference population, while edentulous elder popula- associated with grip strength and sarcopenia, and most
tion over 65 years of age demonstrated no extra risk of of these studies are observational and cross-sectional
mortality. In contrast, a retrospective study among 1385 [37–39]. The predictive value of tooth loss on future sar-
elderly individuals > 75 years old from Shanghai, China copenia in older adults are still unknown. Our findings
found tooth loss was the potential predictors of mortal- help address this gap illustrating that complete edentu-
ity [35]. Compared to elder population, total tooth loss lism independently predicts declining grip strength and
at a younger age is more likely to represent cumulative muscle mass over time among participants aged 45 years
exposure to adverse oral and overall health status, and/ or older. Our findings suggest that, in addition to health
or lifetime stressors [36], where the effect of edentulism factors, oral health indicators are important consider-
on mortality is maximized. Our findings suggest that the ations in determining sarcopenia risk status and preven-
provision of routine dental care and other dental public tion strategies in the elderly population.
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